An Evolutionary-Network Model Reveals Stratified Interactions in the V3 Loop of the HIV-1 Envelope
Publication Date
November 23, 2007
Journal
PLOS Computational Biology
Authors
Art F. Y Poon, Fraser I Lewis, Sergei L. Kosakovsky Pond & Simon D. W Frost
Volume
3
Issue
11
Pages
e231
DOI
http://doi.org/10.1371/journal.pcbi.0030231
Publisher URL
http://journals.plos.org/ploscompbiol/article?id=10.1371%2Fjournal.pcbi.0030231
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/18039027
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2082504
Europe PMC
http://europepmc.org/abstract/MED/18039027
Web of Science
000251310000022
Scopus
36948998606
Mendeley
http://www.mendeley.com/research/evolutionarynetwork-model-reveals-stratified-interactions-v3-loop-hiv1-envelope
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Mendeley | Further Information

{"title"=>"An evolutionary-network model reveals stratified interactions in the V3 loop of the HIV-1 envelope", "type"=>"journal", "authors"=>[{"first_name"=>"Art F Y", "last_name"=>"Poon", "scopus_author_id"=>"15073114700"}, {"first_name"=>"Fraser I.", "last_name"=>"Lewis", "scopus_author_id"=>"7202262525"}, {"first_name"=>"Sergei L.", "last_name"=>"Kosakovsky Pond", "scopus_author_id"=>"7801633431"}, {"first_name"=>"Simon D W", "last_name"=>"Frost", "scopus_author_id"=>"7102366418"}], "year"=>2007, "source"=>"PLoS Computational Biology", "identifiers"=>{"isbn"=>"1553-7358", "doi"=>"10.1371/journal.pcbi.0030231", "pui"=>"350241951", "sgr"=>"36948998606", "scopus"=>"2-s2.0-36948998606", "pmid"=>"18039027", "issn"=>"1553734X"}, "id"=>"3a6b5c2b-a60e-3408-b139-1b8eb096dd3c", "abstract"=>"The third variable loop (V3) of the human immunodeficiency virus type 1 (HIV-1) envelope is a principal determinant of antibody neutralization and progression to AIDS. Although it is undoubtedly an important target for vaccine research, extensive genetic variation in V3 remains an obstacle to the development of an effective vaccine. Comparative methods that exploit the abundance of sequence data can detect interactions between residues of rapidly evolving proteins such as the HIV-1 envelope, revealing biological constraints on their variability. However, previous studies have relied implicitly on two biologically unrealistic assumptions: (1) that founder effects in the evolutionary history of the sequences can be ignored, and; (2) that statistical associations between residues occur exclusively in pairs. We show that comparative methods that neglect the evolutionary history of extant sequences are susceptible to a high rate of false positives (20%-40%). Therefore, we propose a new method to detect interactions that relaxes both of these assumptions. First, we reconstruct the evolutionary history of extant sequences by maximum likelihood, shifting focus from extant sequence variation to the underlying substitution events. Second, we analyze the joint distribution of substitution events among positions in the sequence as a Bayesian graphical model, in which each branch in the phylogeny is a unit of observation. We perform extensive validation of our models using both simulations and a control case of known interactions in HIV-1 protease, and apply this method to detect interactions within V3 from a sample of 1,154 HIV-1 envelope sequences. Our method greatly reduces the number of false positives due to founder effects, while capturing several higher-order interactions among V3 residues. By mapping these interactions to a structural model of the V3 loop, we find that the loop is stratified into distinct evolutionary clusters. We extend our model to detect interactions between the V3 and C4 domains of the HIV-1 envelope, and account for the uncertainty in mapping substitutions to the tree with a parametric bootstrap.", "link"=>"http://www.mendeley.com/research/evolutionarynetwork-model-reveals-stratified-interactions-v3-loop-hiv1-envelope", "reader_count"=>100, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>6, "Student > Doctoral Student"=>1, "Researcher"=>37, "Student > Ph. D. Student"=>21, "Student > Postgraduate"=>6, "Student > Master"=>8, "Other"=>2, "Student > Bachelor"=>8, "Lecturer"=>2, "Professor"=>9}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>6, "Student > Doctoral Student"=>1, "Researcher"=>37, "Student > Ph. D. Student"=>21, "Student > Postgraduate"=>6, "Student > Master"=>8, "Other"=>2, "Student > Bachelor"=>8, "Lecturer"=>2, "Professor"=>9}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Agricultural and Biological Sciences"=>59, "Arts and Humanities"=>1, "Veterinary Science and Veterinary Medicine"=>1, "Chemistry"=>2, "Computer Science"=>10, "Engineering"=>1, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>9, "Mathematics"=>3, "Medicine and Dentistry"=>6, "Physics and Astronomy"=>2, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>6}, "Physics and Astronomy"=>{"Physics and Astronomy"=>2}, "Mathematics"=>{"Mathematics"=>3}, "Unspecified"=>{"Unspecified"=>3}, "Environmental Science"=>{"Environmental Science"=>1}, "Arts and Humanities"=>{"Arts and Humanities"=>1}, "Engineering"=>{"Engineering"=>1}, "Chemistry"=>{"Chemistry"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>59}, "Computer Science"=>{"Computer Science"=>10}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>9}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Argentina"=>1, "United States"=>6, "United Kingdom"=>3, "Switzerland"=>1, "Spain"=>2, "Canada"=>1, "Netherlands"=>2, "Sweden"=>2, "Belgium"=>1, "Brazil"=>3, "Mexico"=>1, "Italy"=>1, "Slovenia"=>1, "Chile"=>1}, "group_count"=>3}

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Scopus | Further Information

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  • {"files"=>["https://ndownloader.figshare.com/files/941386"], "description"=>"<p>A three-dimensional visualization of the structure of the V3 loop, using structural coordinates from a model comprised of the HIV-1 gp120 core protein complexed to the CD4 receptor and the X5 antibody [<a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.0030231#pcbi-0030231-b028\" target=\"_blank\">28</a>]. The structure is oriented such that the host cell membrane would be positioned at the top of the figure. The cysteine residues forming a disulfide bridge that closes the loop are labeled in green. The amino acid sequence depicted here differs from our consensus sequence at five positions, such that identity would require the following substitutions: Q5N, H12R, R17Q, T21A, and E24D.</p>", "links"=>[], "tags"=>["v3"], "article_id"=>611812, "categories"=>["Virology", "Biological Sciences", "Evolutionary Biology"], "users"=>["Art F. Y Poon", "Fraser I Lewis", "Sergei L. Kosakovsky Pond", "Simon D. W Frost"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.0030231.g004", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Structural_Model_of_the_V3_Loop_/611812", "title"=>"Structural Model of the V3 Loop", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-11-23 00:30:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/941470"], "description"=>"<p>A consensus network assembled from edges with marginal posterior probabilities exceeding 0.95, in which nodes represent nonsynonymous substitution events at codon sites in the V3 and C4 domains. Nodes that correspond to residues in the C4 domain are shaded blue (numbered according to their position in the consensus <i>env</i> gene sequence), and nodes that were connected by strongly supported edges in the V3-specific network are shaded black. We retain the same numbering scheme for residues in V3 for consistency.</p>", "links"=>[], "tags"=>["v3", "c4"], "article_id"=>611893, "categories"=>["Virology", "Biological Sciences", "Evolutionary Biology"], "users"=>["Art F. Y Poon", "Fraser I Lewis", "Sergei L. Kosakovsky Pond", "Simon D. W Frost"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.0030231.g005", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Combined_V3_and_C4_Network_/611893", "title"=>"Combined V3 and C4 Network", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-11-23 00:31:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/941167"], "description"=>"<div><p>(A) A receiver operating characteristic (ROC)-like curve, in which the <i>y</i>-axis corresponds to the true-positive rate (TPR), and the <i>x</i>-axis corresponds to the false-positive rate (FPR). A perfect analytical method would be located in the upper-left corner (i.e., TPR = 1, FPR = 0), whereas methods located near the diagonal (dashed line, TPR = FPR) are statistically equivalent to a random guess. Each point in the plot corresponds to the mean outcome from the corresponding model analysis (orange = the Fisher exact test, black = evolutionary-network) of ten replicate simulations of binary-state sequences evolving under various settings of the pairwise coevolution parameter, ɛ (ranging from 1 to 3; see figure labels).</p><p>(B) Boxplots corresponding to the false-positive rate (as a fraction of the total number of pairwise comparisons = 528) from the corresponding analysis (evolutionary-network [Evol-Net] or Fisher exact test [Fisher]) of simulated sequences evolving according to a null model of codon substitutions in which sites evolve independently, using parameter settings estimated from the original V3 sequence alignment. We generated 100 replicate simulations of nucleotide sequences evolving along the original neighbor-joining tree.</p></div>", "links"=>[], "tags"=>["false-positive", "rates", "simulated"], "article_id"=>611591, "categories"=>["Virology", "Biological Sciences", "Evolutionary Biology"], "users"=>["Art F. Y Poon", "Fraser I Lewis", "Sergei L. Kosakovsky Pond", "Simon D. W Frost"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.0030231.g001", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_True_and_False_Positive_Rates_on_Simulated_Data_/611591", "title"=>"True- and False-Positive Rates on Simulated Data", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-11-23 00:26:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/941312"], "description"=>"<p>Each node corresponds to a residue in the V3 loop, numbered according to their position in the consensus sequence (identical to Korber et al. [<a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.0030231#pcbi-0030231-b019\" target=\"_blank\">19</a>]) and labeled with the consensus amino acid. Dark-shaded nodes indicate residues that are connected by edges with parametric bootstrap support values exceeding 50%; each edge is labeled with its support value. Edges with support values below this threshold are indicated by dashed lines.</p>", "links"=>[], "tags"=>["v3"], "article_id"=>611737, "categories"=>["Virology", "Biological Sciences", "Evolutionary Biology"], "users"=>["Art F. Y Poon", "Fraser I Lewis", "Sergei L. Kosakovsky Pond", "Simon D. W Frost"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.0030231.g003", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_Consensus_Network_of_V3_Residues_/611737", "title"=>"The Consensus Network of V3 Residues", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-11-23 00:28:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/463676", "https://ndownloader.figshare.com/files/463680", "https://ndownloader.figshare.com/files/463686", "https://ndownloader.figshare.com/files/463692"], "description"=>"<div><p>The third variable loop (V3) of the human immunodeficiency virus type 1 (HIV-1) envelope is a principal determinant of antibody neutralization and progression to AIDS. Although it is undoubtedly an important target for vaccine research, extensive genetic variation in V3 remains an obstacle to the development of an effective vaccine. Comparative methods that exploit the abundance of sequence data can detect interactions between residues of rapidly evolving proteins such as the HIV-1 envelope, revealing biological constraints on their variability. However, previous studies have relied implicitly on two biologically unrealistic assumptions: (1) that founder effects in the evolutionary history of the sequences can be ignored, and; (2) that statistical associations between residues occur exclusively in pairs. We show that comparative methods that neglect the evolutionary history of extant sequences are susceptible to a high rate of false positives (20%–40%). Therefore, we propose a new method to detect interactions that relaxes both of these assumptions. First, we reconstruct the evolutionary history of extant sequences by maximum likelihood, shifting focus from extant sequence variation to the underlying substitution events. Second, we analyze the joint distribution of substitution events among positions in the sequence as a Bayesian graphical model, in which each branch in the phylogeny is a unit of observation. We perform extensive validation of our models using both simulations and a control case of known interactions in HIV-1 protease, and apply this method to detect interactions within V3 from a sample of 1,154 HIV-1 envelope sequences. Our method greatly reduces the number of false positives due to founder effects, while capturing several higher-order interactions among V3 residues. By mapping these interactions to a structural model of the V3 loop, we find that the loop is stratified into distinct evolutionary clusters. We extend our model to detect interactions between the V3 and C4 domains of the HIV-1 envelope, and account for the uncertainty in mapping substitutions to the tree with a parametric bootstrap.</p></div>", "links"=>[], "tags"=>["evolutionary-network", "reveals", "stratified", "interactions", "v3", "hiv-1"], "article_id"=>151386, "categories"=>["Biological Sciences", "Cancer", "Evolutionary Biology"], "users"=>["Art F. Y Poon", "Fraser I Lewis", "Sergei L. Kosakovsky Pond", "Simon D. W Frost"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.0030231.sg001", "https://dx.doi.org/10.1371/journal.pcbi.0030231.sg002", "https://dx.doi.org/10.1371/journal.pcbi.0030231.sg003", "https://dx.doi.org/10.1371/journal.pcbi.0030231.st001"], "stats"=>{"downloads"=>21, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/An_Evolutionary_Network_Model_Reveals_Stratified_Interactions_in_the_V3_Loop_of_the_HIV_1_Envelope/151386", "title"=>"An Evolutionary-Network Model Reveals Stratified Interactions in the V3 Loop of the HIV-1 Envelope", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2007-11-23 00:23:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/941239"], "description"=>"<p>This histogram indicates the frequency of the marginal posterior probability of the 528 possible edges, sampled from a Markov chain over the space of node orders (see <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.0030231#s2\" target=\"_blank\">Materials and Methods</a>). The prior probability of each edge was set to the uninformative value of 0.5. Note that the vertical range of the histogram was truncated to a maximum of 50; the first bin of the histogram contained 485 edges as indicated on the figure. Individual values are indicated by tick marks along the <i>x</i>-axis. A red line indicates the arbitrary cutoff value of 0.95.</p>", "links"=>[], "tags"=>["marginal", "posterior", "probability"], "article_id"=>611663, "categories"=>["Virology", "Biological Sciences", "Evolutionary Biology"], "users"=>["Art F. Y Poon", "Fraser I Lewis", "Sergei L. Kosakovsky Pond", "Simon D. W Frost"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.0030231.g002", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Distribution_of_the_Marginal_Posterior_Probability_of_Network_Edges_/611663", "title"=>"Distribution of the Marginal Posterior Probability of Network Edges", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-11-23 00:27:43"}

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